Scale-free movement patterns in termites emerge from social interactions and preferential attachments.

As the number or density of interacting individuals in a social group increases, a transition can develop from uncorrelated and disordered behavior of the individuals to a collective coherent pattern. We expand this observation by exploring the fine details of termite movement patterns to demonstrate that the value of the scaling exponent µ of a power law describing the Lévy walk of an individual is modified collectively as the density of animals in the group changes. This effect is absent when termites interact with inert obstacles. We also show that the network of encounters and interactions among specific individuals is selective, resembling a preferential attachment mechanism that is important for social networking. Our data strongly suggest that preferential attachments, a phenomenon not reported previously, and favorite interactions with a limited number of acquaintances are responsible for the generation of Lévy movement patterns in these social insects.

Social context modulates scale-free movements in a social insect.

Most animals move intermittently, pausing or slowing down for short moments and short moves, and darting away towards a new location where to hover again. This pattern occurs at a range of spatial and temporal scales (thence, resembling 'scale-free'), from the quick inspection of local areas to the sum of all movements performed from birth to death. While this pattern has been extensively described, its proximate drivers remain open to debate. A current hypothesis states that underlying proximate generative mechanisms of intermittent movement of animals are linked to external stimuli, e.g., interactions with the abiotic environment, resources, and other individuals. Here we investigated a prediction from this hypothesis, using termites as a biological model. We verified whether the social background in which a termite is inserted will modify the parameters of its intermittent scale-free spatial displacement. This relates to the hypothesis because it inspects how do external stimuli coming from intraspecifics can affect this type of movement. We tracked the trajectories of a focal termite confined along its nestmates in experimental clueless arenas, every 0.5 s along about six hours. Arenas varied in group size and comprised 22 distinct caste compositions, yielding 75 trackings (> 400 h) and more than two million Cartesian coordinates. Most of these trajectories (96% or 72/75) were classified as intermittent scale free (Lévy-like), indicating prevalence of this type of movement over non-Lévy-like ones (P=1.62×10-15). Moreover, intermittent scale-free movements performed by the focal termite (i) did arise outside the foraging-searching framework, and (ii) were modified by the social context while remaining within the limits of Lévy-walk realms. That is, some limits seem to exist along with the necessary plasticity to provide room for natural selection. Moreover, by arising outside the foraging framework, Lévy-like movements are shown to have broader relevance. Studies on processes that depend on social context and movement (e.g., collective behaviour, the spread of diseases) may, hence, profit from such concepts.

Metal bioaccumulation alleviates the negative effects of herbivory on plant growth.

Metalliferous soils can selectively shape plant species' physiology towards tolerance of high metal concentrations that are usually toxic to organisms. Some adapted plant species tolerate and accumulate metal in their tissues. These metals can serve as an elemental defence but can also decrease growth. Our investigation explored the capacity of natural metal accumulation in a tropical tree species, Eremanthus erythropappus (Asteraceae) and the effects of such bioaccumulation on plant responses to herbivory. Seedlings of E. erythropappus were grown in a glasshouse on soils that represented a metal concentration gradient (Al, Cu, Fe, Mn and Zn), and then the exposed plants were fed to the herbivores in a natural habitat. The effect of herbivory on plant growth was significantly mediated by foliar metal ion concentrations. The results suggest that herbivory effects on these plants change from negative to positive depending on soil metal concentration. Hence, these results provide quantitative evidence for a previously unsuspected interaction between herbivory and metal bioaccumulation on plant growth.

Nonaggressive behavior: A strategy employed by an obligate nest invader to avoid conflict with its host species.

In addition to its builders, termite nests are known to house a variety of secondary opportunistic termite species so-called inquilines, but little is known about the mechanisms governing the maintenance of these symbioses. In a single nest, host and inquiline colonies are likely to engage in conflict due to nestmate discrimination, and an intriguing question is how both species cope with each other in the long term. Evasive behaviour has been suggested as one of the mechanisms reducing the frequency of host-inquiline encounters, yet, the confinement imposed by the nests' physical boundaries suggests that cohabiting species would eventually come across each other. Under these circumstances, it is plausible that inquilines would be required to behave accordingly to secure their housing. Here, we show that once inevitably exposed to hosts individuals, inquilines exhibit nonthreatening behaviours, displaying hence a less threatening profile and preventing conflict escalation with their hosts. By exploring the behavioural dynamics of the encounter between both cohabitants, we find empirical evidence for a lack of aggressiveness by inquilines towards their hosts. Such a nonaggressive behaviour, somewhat uncommon among termites, is characterised by evasive manoeuvres that include reversing direction, bypassing and a defensive mechanism using defecation to repel the host. The behavioural adaptations we describe may play an important role in the stability of cohabitations between host and inquiline termite species: by preventing conflict escalation, inquilines may improve considerably their chances of establishing a stable cohabitation with their hosts.

Individual basis for collective behaviour in the termite, Cornitermes cumulans.

Interactions among individuals in social groups lead to the emergence of collective behaviour at large scales by means of multiplicative non-linear effects. Group foraging, nest building and task allocation are just some well-known examples present in social insects. However the precise mechanisms at the individual level that trigger and amplify social phenomena are not fully understood. Here we show evidence of complex dynamics in groups of the termite, Cornitermes cumulans (Kollar) (Isoptera: Termitidae), of different sizes and qualitatively compare the behaviour observed with that exhibited by agent-based computer models. It is then concluded that certain aspects of social behaviour in insects have a universal basis common to interconnected systems and that this may be useful for understanding the temporal dynamics of systems displaying social behaviour in general.

Disturbance-modulated symbioses in termitophily.

Symbiosis, the living-together of unlike organisms, underlies every major transition in evolution and pervades most ecological dynamics. Among examples of symbioses, the simultaneous occupation of a termite nest by its builder termites and intruding invertebrate species (so-called termitophily) provides suitable macroscopic scenarios for the study of species coexistence in confined environments. Current evidence on termitophily abounds for dynamics occurring at the interindividual level within the termitarium, but is insufficient for broader scales such as the community and the landscape. Here, we inspect the effects of abiotic disturbance on termitophile presence and function in termitaria at these broader scales. To do so, we censused the termitophile communities inhabiting 30 termitaria of distinct volumes which had been exposed to increasing degrees of fire-induced disturbance in a savanna-like ecosystem in southeastern Brazil. We provide evidence that such an abiotic disturbance can ease the living-together of termitophiles and termites. Putative processes facilitating these symbioses, however, varied according to the invader. For nonsocial invaders, disturbance seemed to boost coexistence with termites via the habitat amelioration that termitaria provided under wildfire, as suggested by the positive correlation between disturbance degree and termitophile abundance and richness. As for social invaders (ants), disturbance seemed to enhance associational defenses with termites, as suggested by the negative correlation between the presence of ant colonies and the richness and abundance of other termitarium-cohabiting termitophiles. It is then apparent that disturbance-modulated distinct symbioses in these termite nests.

Top-down network analysis characterizes hidden termite-termite interactions.

The analysis of ecological networks is generally bottom-up, where networks are established by observing interactions between individuals. Emergent network properties have been indicated to reflect the dominant mode of interactions in communities that might be mutualistic (e.g., pollination) or antagonistic (e.g., host-parasitoid communities). Many ecological communities, however, comprise species interactions that are difficult to observe directly. Here, we propose that a comparison of the emergent properties from detail-rich reference communities with known modes of interaction can inform our understanding of detail-sparse focal communities. With this top-down approach, we consider patterns of coexistence between termite species that live as guests in mounds built by other host termite species as a case in point. Termite societies are extremely sensitive to perturbations, which precludes determining the nature of their interactions through direct observations. We perform a literature review to construct two networks representing termite mound cohabitation in a Brazilian savanna and in the tropical forest of Cameroon. We contrast the properties of these cohabitation networks with a total of 197 geographically diverse mutualistic plant-pollinator and antagonistic host-parasitoid networks. We analyze network properties for the networks, perform a principal components analysis (PCA), and compute the Mahalanobis distance of the termite networks to the cloud of mutualistic and antagonistic networks to assess the extent to which the termite networks overlap with the properties of the reference networks. Both termite networks overlap more closely with the mutualistic plant-pollinator communities than the antagonistic host-parasitoid communities, although the Brazilian community overlap with mutualistic communities is stronger. The analysis raises the hypothesis that termite-termite cohabitation networks may be overall mutualistic. More broadly, this work provides support for the argument that cryptic communities may be analyzed via comparison to well-characterized communities.

Allometric Scaling of Patrolling Rate and Nest Volume in Constrictotermes cyphergaster Termites: Hints on the Settlement of Inquilines.

Structural and functional traits of organisms are known to be related to the size of individuals and to the size of their colonies when they belong to one. Among such traits, propensity to inquilinism in termites is known to relate positively to colony size. Larger termitaria hold larger diversity of facultative inquilines than smaller nests, whereas obligate inquilines seem unable to settle in nests smaller than a threshold volume. Respective underlying mechanisms, however, remain hypothetical. Here we test one of such hypotheses, namely, that nest defence correlates negatively to nest volume in Constrictotermes cyphergaster termites (Termitidae: Nasutitermitinae). As a surrogate to defence, we used 'patrolling rate', i.e., the number of termite individuals attending per unit time an experimentally damaged spot on the outer wall of their termitaria. We found that patrolling rate decayed allometrically with increasing nest size. Conspicuously higher patrolling rates occurred in smaller nests, while conspicuously lower rates occurred in larger nests presenting volumes in the vicinity of the threshold value for the establishment of inquilinism. This could be proven adaptive for the host and guest. At younger nest age, host colonies are smaller and presumably more vulnerable and unstable. Enhanced defence rates may, hence, prevent eventual risks to hosts from inquilinism at the same time that it prevents inquilines to settle in a still unstable nest. Conversely, when colonies grow and maturate enough to stand threats, they would invest in priorities other than active defence, opening an opportunity for inquilines to settle in nests which are more suitable or less risky. Under this two-fold process, cohabitation between host and inquiline could readily stabilize.

The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae): the integration of chemical and vibroacoustic signals.

Alarm signalling is of paramount importance to communication in all social insects. In termites, vibroacoustic and chemical alarm signalling are bound to operate synergistically but have never been studied simultaneously in a single species. Here, we inspected the functional significance of both communication channels in Constrictotermes cyphergaster (Termitidae: Nasutitermitinae), confirming the hypothesis that these are not exclusive, but rather complementary processes. In natural situations, the alarm predominantly attracts soldiers, which actively search for the source of a disturbance. Laboratory testing revealed that the frontal gland of soldiers produces a rich mixture of terpenoid compounds including an alarm pheromone. Extensive testing led to identification of the alarm pheromone being composed of abundant monoterpene hydrocarbons (1S)-α-pinene and myrcene, along with a minor component, (E)-ß-ocimene. The vibratory alarm signalling consists of vibratory movements evidenced as bursts; a series of beats produced predominantly by soldiers. Exposing termite groups to various mixtures containing the alarm pheromone (crushed soldier heads, frontal gland extracts, mixture of all monoterpenes, and the alarm pheromone mixture made of standards) resulted in significantly higher activity in the tested groups and also increased intensity of the vibratory alarm communication, with the responses clearly dose-dependent. Lower doses of the pheromone provoked higher numbers of vibratory signals compared to higher doses. Higher doses induced long-term running of all termites without stops necessary to perform vibratory behaviour. Surprisingly, even crushed worker heads led to low (but significant) increases in the alarm responses, suggesting that other unknown compound in the worker's head is perceived and answered by termites. Our results demonstrate the existence of different alarm levels in termites, with lower levels being communicated through vibratory signals, and higher levels causing general alarm or retreat being communicated through the alarm pheromone.

Lévy flights and self-similar exploratory behaviour of termite workers: beyond model fitting.

Animal movements have been related to optimal foraging strategies where self-similar trajectories are central. Most of the experimental studies done so far have focused mainly on fitting statistical models to data in order to test for movement patterns described by power-laws. Here we show by analyzing over half a million movement displacements that isolated termite workers actually exhibit a range of very interesting dynamical properties--including Lévy flights--in their exploratory behaviour. Going beyond the current trend of statistical model fitting alone, our study analyses anomalous diffusion and structure functions to estimate values of the scaling exponents describing displacement statistics. We evince the fractal nature of the movement patterns and show how the scaling exponents describing termite space exploration intriguingly comply with mathematical relations found in the physics of transport phenomena. By doing this, we rescue a rich variety of physical and biological phenomenology that can be potentially important and meaningful for the study of complex animal behavior and, in particular, for the study of how patterns of exploratory behaviour of individual social insects may impact not only their feeding demands but also nestmate encounter patterns and, hence, their dynamics at the social scale.

Mutual use of trail-following chemical cues by a termite host and its inquiline.

Termite nests are often secondarily inhabited by other termite species ( = inquilines) that cohabit with the host. To understand this association, we studied the trail-following behaviour in two Neotropical species, Constrictotermes cyphergaster (Termitidae: Nasutitermitinae) and its obligatory inquiline, Inquilinitermes microcerus (Termitidae: Termitinae). Using behavioural experiments and chemical analyses, we determined that the trail-following pheromone of C. cyphergaster is made of neocembrene and (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol. Although no specific compound was identified in I. microcerus, workers were able to follow the above compounds in behavioural bioassays. Interestingly, in choice tests, C. cyphergaster prefers conspecific over heterospecific trails while I. microcerus shows the converse behaviour. In no-choice tests with whole body extracts, C. cyphergaster showed no preference for, while I. microcerus clearly avoided heterospecific trails. This seems to agree with the hypothesis that trail-following pheromones may shape the cohabitation of C. cyphergaster and I. microcerus and reinforce the idea that their cohabitation is based on conflict-avoiding strategies.

Diet Segregation between Cohabiting Builder and Inquiline Termite Species.

How do termite inquilines manage to cohabit termitaria along with the termite builder species? With this in mind, we analysed one of the several strategies that inquilines could use to circumvent conflicts with their hosts, namely, the use of distinct diets. We inspected overlapping patterns for the diets of several cohabiting Neotropical termite species, as inferred from carbon and nitrogen isotopic signatures for termite individuals. Cohabitant communities from distinct termitaria presented overlapping diet spaces, indicating that they exploited similar diets at the regional scale. When such communities were split into their components, full diet segregation could be observed between builders and inquilines, at regional (environment-wide) and local (termitarium) scales. Additionally, diet segregation among inquilines themselves was also observed in the vast majority of inspected termitaria. Inquiline species distribution among termitaria was not random. Environmental-wide diet similarity, coupled with local diet segregation and deterministic inquiline distribution, could denounce interactions for feeding resources. However, inquilines and builders not sharing the same termitarium, and thus not subject to potential conflicts, still exhibited distinct diets. Moreover, the areas of the builder's diet space and that of its inquilines did not correlate negatively. Accordingly, the diet areas of builders which hosted inquilines were in average as large as the areas of builders hosting no inquilines. Such results indicate the possibility that dietary partitioning by these cohabiting termites was not majorly driven by current interactive constraints. Rather, it seems to be a result of traits previously fixed in the evolutionary past of cohabitants.

[Does vegetational diversification reduce coffee leaf miner Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae) attack?]. / A diversificação da vegetação reduz o ataque do bicho-mineiro-do-cafeeiro Leucoptera coffeella (Guérin-mèneville) (Lepidoptera: Lyonetiidae)?

The effects of increasing plant diversity on the population of the coffee leaf-miner Leucoptera coffeella (Guérin-Mèneville) were investigated in two organic coffee production systems. One system consisted of coffee intercropped with banana trees (shaded system) and the other one of coffee intercropped with pigeon pea (unshaded system). The increase in plant diversity on both systems was achieved via introduction of green manures such a perennial pea nut, sunn hemp and Brazilian lucerne. The population of L. coffeella, predation and parasitism of L. coffeella mines were biweekly evaluated during eight months. The increase in plant diversity on both systems did not affect the attack of L. coffeella on coffee leaves and the mine parasitism rate. However, there was a positive and significant relationship between increasing plant diversity and coffee leaf mine predation by wasps on unshaded coffee system and a negative relationship on shaded coffee system.

A diversificação da vegetação reduz o ataque do bicho-mineiro-do-cafeeiro Leucoptera coffeella (Guérin-mèneville) (Lepidoptera: Lyonetiidae)? / Does vegetational diversification reduce coffee leaf miner Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae) attack?

The effects of increasing plant diversity on the population of the coffee leaf-miner Leucoptera coffeella (Guérin-Mèneville) were investigated in two organic coffee production systems. One system consisted of coffee intercropped with banana trees (shaded system) and the other one of coffee intercropped with pigeon pea (unshaded system). The increase in plant diversity on both systems was achieved via introduction of green manures such a perennial pea nut, sunn hemp and Brazilian lucerne. The population of L. coffeella, predation and parasitism of L. coffeella mines were biweekly evaluated during eight months. The increase in plant diversity on both systems did not affect the attack of L. coffeella on coffee leaves and the mine parasitism rate. However, there was a positive and significant relationship between increasing plant diversity and coffee leaf mine predation by wasps on unshaded coffee system and a negative relationship on shaded coffee system.

Reproduction and survival of Muscina stabulans under laboratory conditions / Reprodução e sobrevivência de Muscina stabulans em condições de laboratório

This is the first published report concerning reproduction and survival using life table analyses of fertility and survival for Muscina stabulans maintained under laboratory conditions with artificial diets. The intrinsic rate of growth, reproduction rate and average generational time were obtained, suggesting a rapid population growth under these rearing conditions. These findings permitted the creation of time models of survival and oviposition, as well as a quantitative estimate of the adaptation capacity of this species.

Com o objetivo de apresentar um primeiro delineamento para a reprodução e sobrevivência da Muscina stabulans em condições de laboratório, foram desenvolvidas tabelas de vida em dieta artificial. A taxa intrínseca de crescimento natural, a taxa reprodutiva líquida e o tempo médio de uma geração foram estimados, além da análise do tempo de oviposição e da sobrevivência dos adultos dessa espécie. Os dados sugerem uma alta taxa de crescimento da população nas condições de criação. Esses resultados permitem a criação de modelos de sobrevivência e oviposição, bem como estimativas quantitativas da adaptabilidade dessa espécie.

Efeito da profundidade de aplicação e da distribuição de inseticidas líquidos no controle de cupins de montículo em pastagens (Isoptera: Termitidae) / The effects of depth and distribution of liquid insecticides for the control of mound termites in pastures (Isoptera: Termitidae)

Foi testada a eficiência de duas profundidades de aplicação de cupinicidas líquidos para o controle de cupins de montículo Cornitermes sp. (Isoptera: Termitidae) em pastagens na região Sul de Minas Gerais. Estes aplicadores diferiam basicamente quanto à profundidade e distribuição da calda cupinicida dentro do ninho, sendo um aplicador de tubo curto e outro de tubo longo e perfurado. Os resultados mostram que, o aplicador e tubo longo e perfurado apresenta maior eficiência de controle de cupins de montículo em pastagem e que a profundidade e distribuição de aplicação da calda cupinicida interfere na taxa de mortalidade das colônias. O uso de um aplicador com tubo longo, pode ser uma estratégia adequada para o efetivo controle de cupins de montículo, quando se utilizam inseticidas em formulação líquida.

The efficacy of two depths was tested for the control of mound termites, Cornitermes sp. (Isoptera: Termitidae) using liquid a formulation of imidacloprid. Both devices were funnels constructed so as to differ only in the depth and distribution of the liquid within the termite nest. One of the devices was a standard funnel, whereas the other presented a longer tube perforated along its extension and closed in the outer end. Termites in mounds treated with the long funnel died faster than termites treated with the short funnel. It seems that the depth and distribution of the insecticide within termite nest was crucial for the efficacy of the control. We therefore recommend that control methods of termite in mounds should favor the use of applying devices which distribute better the insecticide within the nest.